Changes in soil quality due to converting Pinus to Eucalyptus plantations and subsequent successive Eucalyptus planting in southern China

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Introduction
Vegetation plays a key role in soil development due to its influence on nutrient cycling, hydrological processes and soil erosion (de la Paix et al., 2013;Zhao et al., 2013).

Soil degradation caused by deforestation is a serious problem and afforestation is of-Figures Back Close
Full ten recommended as an effective way to protect soil surface and improve soil quality (Miao et al., 2012;Zhao et al., 2013), as well as produce timber.Eucalyptus is an important tree species for afforestation in tropical or subtropical regions and has been introduced to many countries around the world.In southern China, millions of hectares of degraded land, cropland and natural secondary forest have been converted into Eucalyptus plantations and successive planting has been undertaken (Wen et al., 2009).However, due to nutrient limitations in many areas (LeBauer and Treseder, 2008) and a high demand for nutrients by Eucalyptus (Laclau et al., 2010), this kind of land use change may exhaust soil nutrients and decrease soil quality.Inappropriate plantation management also accelerates the decline in soil quality (Yu et al., 2009).There is an urgent need to assess the effects that Eucalyptus planting has on soil quality since it plays a key role in sustaining forest productivity.Soil quality includes soil physical, chemical and biological properties, as well as soil processes and their interactions (Andrews and Carroll, 2001).Many studies have focused on soil physicochemical properties (Garay et al., 2004), microbial communities (Wu et al., 2012) or enzyme activities (Wang et al., 2008), which only reflect some aspects of soil quality.The soil quality index (SQI) provides a tool for quantifying the combined biological, chemical and physical response of soil to land use and soil/crop management practices (Andrews and Carroll, 2001;Andrews et al., 2002).It provides an intelligible and more holistic measurement of soil quality and, in recent years, the SQI has been used to assess the impacts of land use change, forest and cropland management and ecological restoration (Navas et al., 2011).Methods used to calculate SQI include expert opinion and principal component analysis (PCA) (Andrews et al., 2002), with the latter more widely used in recent studies (Navas et al., 2011).
The ecological consequences of Eucalyptus planting are important and have been studied in depth.Some studies have reported that soil organic carbon, nitrogen, microbial biomass and the metabolic quotient were significantly lower in Eucalyptus plantations compared to natural and regenerated forests or pastures (Behera and Sahani, 2003;Chen et al., 2013;Sicardi et al., 2004;Araújo et al., 2010).However, other stud-Introduction

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Full ies have found that the conversion of native savanna or sugarcane fields to Eucalyptus plantations did not change soil total organic carbon, microbial biomass carbon or nitrogen levels (Binkley et al., 2004).Fialho and Zinn (2012) compiled paired-plot studies on how SOC stocks under native vegetation change after planting fast-growth Eucalyptus species in Brazil and found that Eucalyptus plantations on average had no net effect on soil organic carbon stocks.The results of these different studies were not consistent and the effect of successive Eucalyptus planting has rarely been reported.
In order to access the effects of converting Pinus to Eucalyptus and subsequent successive Eucalyptus planting on soil quality, we selected adjacent plantations of local Pinus massoniana Lamb.(Pinus) and 1st, 2nd, 3rd and 4th generations of Eucalyptus urophylla × grandis (Eucalyptus) in Guangxi, China.The changes in soil quality were investigated by measuring the soil chemical and biological properties and by calculating a SQI using the PCA method for each plantation.Considering soil nutrients exhaustion was the main problem in Eucalyptus plantation, the soil physical attributes were not considered in this study.We hypothesized that (1) converting Pinus to Eucalyptus plantations would significantly decrease soil quality, and (2) soil quality would continue to decrease with successive Eucalyptus planting.

Study area
This study was conducted at Fusui, Guangxi, China (22 • 14 -22 • 21 N, 107 • 47 -107 • 56 E).The altitudes of our study sites were between 140 and 250 m a.s.l., the slope aspects were southeast and the slope angles were less than 15 • .The region has a typical subtropical monsoon climate with mean annual temperatures of 21.2-22.3 • C.
The rainfall is 1100-1300 mm per year, concentrated during June-August.Soils in the region are mainly lateritic red earth with soil depth of 80 cm or more and are derived from arenaceous shale with a pH ranging from 4 to 5. Introduction

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Full This area was dominated by Pinus until the end of the 1970s and had a rotation of about 30 years.No management practices were carried out in the Pinus plantations, except lacerating the tree bark for oil.However, over time, fast-growing Eucalyptus began to replace Pinus and it has become the dominant tree species in this area.Clear-cutting and fire clearance were carried out during the conversion of Pinus to Eucalyptus plantations and full reclamation (plowed to 50 cm depth) was conducted prior to Eucalyptus planting (1st generation) with seedlings.The tree density in the Eucalyptus plantations was 1250-1667 trees ha −1 and there was a 5 year rotation period.The 2nd generation Eucalyptus was regenerated by sprouts without plowing.After strip reclamation (plowed to 50 cm depth), the 3rd generation Eucalyptus was planted with seedlings.
The 4th generation was regenerated by sprouts without plowing.The surface soil was bare for about 2 months before Eucalyptus seedling planting.During the crop transition periods, soil erosion happened easily due to the lack of vegetation protection.Before planting, base fertilizer (500 g seedling −1 , N : P : K = 10 : 15 : 5) was put into a 20 cm deep soil hole and covered with soil.At 6, 12 and 24 months after planting, 250, 500 and 500 g, respectively, of fertilizer (N : P : K = 15 : 10 : 8) per tree was separately applied in soil holes that were 30 cm away from each tree.The application of herbicide (glyphosate) was performed once a year during the first 3 years after Eucalyptus planting and consequently the coverage of understory plants was less than 50 %.However, the understory coverage increased gradually in the 4th and 5th year after Eucalyptus planting.The leaf, branch and bark litter were kept in the plantation during the plant growth period, but at harvest time, most branch litter was removed and burned before the next rotation.

Experimental design and sampling
The adjacent plantations of local Pinus and 1st, 2nd, 3rd and 4th generations of Eucalyptus at the Dongmen Forestry Farm were selected to represent Pinus planting and 1st, 2nd, 3rd and 4th generations of successive Eucalyptus planting.Three 20 m×20 m plots were marked out in each plantation site.During sampling time, the tree, shrub and Introduction

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Full grass coverage in the Pinus plantation was about 60 %, 25 % and 70 %, respectively.The tree, shrub and grass coverage in the Eucalyptus plantations was similar, about 40 %, 10 % and 45 %, respectively.The litter layer was about 3 cm depth in the Pinus plantation and 1 cm depth in the Eucalyptus plantations.
In October 2010, soil from the top 0-10 cm layer was collected from the study sites.At the time of soil sampling, the ages of Pinus and Eucalyptus were 20 years and 3 years, respectively.Ten soil cores were randomly collected in each plot using a 3.6 cm diameter soil auger and mixed together as a composite sample.Three composite samples were collected at each site.The soil samples were immediately transported to the laboratory.Stones and roots were removed from the soil samples by hand and then the soil samples were sieved through 2 mm sieves.Some soil was stored at 4 • C for soil microbial biomass and enzyme activity analyses, while the remaining soil was air dried for chemical analyses.

Soil chemical and biological analyses
Soil water content was determined gravimetrically after oven-drying at 105 • C for 24 h in order to correct sample weights in biochemical property measurements.Soil pH was measured in deionized water (1 : 2.5 w/v) using a Delta 320 pH-meter (Mettler-Toledo Instruments (Shanghai) Co., Ltd.).Soil organic carbon (SOC) was measured using the Walkley and Black wet oxidation procedure method as outlined in Bao (2000).Soil total nitrogen (TN) was determined by combustion in a Vario EL III Elemental Analyzer (Elementar Analysensysteme GmbH, Germany).Soil alkaline hydrolytic nitrogen (AN) was measured according to Bao (2000). 1 g air-dried soil was incubated in 5 mL sodium hydroxide solution (1.2 M) in the outside ring of an airtight Conway diffusion cell and 3 mL boric acid (0.3 M) was put in the inner well at 40 • C for 24 h.With Methyl redbromocresol green as indicator, 0.01 M hydrochloric acid was used to titrate ammonia absorbed in the boric acid.For total phosphorus (TP) and total potassium (TK), airdried soil samples were digested using 18.4 M sulfuric acid (1 : 10 w/v) and 12.7 M perchloric acid at 275 • C for 6 h, TP and TK were measured using a Prodigy High Dis-Introduction

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Full persion ICP-OES (Teledyne Technologies Incorporated, USA).Available phosphorus (AP) was measured after extraction with 0.05 N sulfuric and 0.025 N hydrochloric acids (1 : 5 w/v) with shaking for 5 min and available potassium (AK) was measured after extraction with 1 N ammonium acetate solution (1 : 10 w/v) with shaking for 30 min (Bao, 2000).AP and AK were measured using the Prodigy High Dispersion ICP-OES.
Soil microbial biomass carbon and nitrogen (MBC and MBN) were estimated using the chloroform fumigation extraction method (Vance et al., 1987).Soil β-glucosidase (BG), phenol oxidase (PO), peroxidase (POD) and acid phosphatase (ACP) activities were measured according to Waldrop et al. (2000).Soil protease (PRO) activity was estimated according to Ladd and Butler (1972).Soil urease (URE) activity was assessed according to Kandeler and Gerber (1988).Soil cellobiosidase (CBH) activity was measured using the fluorimetric method according to Saiya-Cork et al. (2002).Andrews and Carroll (2001).Three steps were involved in the elaboration of this quality index: definition of a minimum data set (MDS), assignment of a score to each indicator by linear scoring functions and data integration into an index.

SQI was calculated according to
Three steps were used to identify the MDS in our study.(1) Data screening.One-way analysis of variance (ANOVA) was performed for soil chemical and biological properties.Only variables with significant differences between treatments (p < 0.05) were chosen for the next step.( 2 well-correlated groups, we summed the absolute values of the correlation coefficients for these variables and assumed that the variable with the highest correlation sum best represented the group.The choice among well-correlated variables was also based on the published references and expert opinion about the soils and sites (Xu, 2000;Wang et al., 2008;Yu et al., 2009).Any uncorrelated, highly weighted variables were considered important and retained in the MDS.Linear scoring was used in our study.Indicators were ranked in ascending or descending order depending on whether a higher value was considered "good" or "bad" in terms of soil function.In our study, all variables were "more is better".The linear scoring function used for converting measured values to scored values is as follows (Zheng et al., 2005): Where S i j is the score of soil variable i of sample j , V i j is the observed variable value of sample j , V i max is the highest value of variable i , and V i min is the lowest value of

S i n
Where S i is the score assigned to indicator i , and n is the number of indicators included in the MDS.

Statistical analyses
We acknowledge that the three 20 m × 20 m plots established per site do not constitute true replicates, because they are located within the same site of the 5 plantations Introduction

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Full (Pinus, 1st, 2nd, 3rd and 4th generations Eucalyptus plantations) and no plots were established in other stands with similar plantation characteristics.Nevertheless, these plantation stands occur in similar topographic conditions and soil parent material, and they were similar in planting history of Pinus plantation before the 1970s.That allowed us to consider the five sites as different treatments.Therefore, one-way variance analyses were used to test the significant differences in soil chemical and biological properties and SQIs among these treatments.Normality of the data was tested using the Kolmogorov-Smirnov test and the soil indicators obeyed standard normal distribution.Tukey's test was used for multiple comparison analysis.All statistical analyses were performed using SPSS 10.0 (SPSS Inc., Chicago, IL, USA) and SigmaPlot for Windows version 11.0 (Systa Software Inc.).

Soil chemical properties
The SOC, TN and AN ranges at our study sites were 10.8-26.9g kg −1 , 0.9-1.6 g kg −1 and 41.4-60.3mg kg −1 , respectively.They were highest in the Pinus plantation, significantly decreased in the 1st and 2nd generations Eucalyptus plantations and then gradually recovered in the 3rd and 4th generations (Fig. 1b, c, and f).SOC and TN in the 4th generation Eucalyptus were significantly lower than in the Pinus plantation, but significantly higher than in the 2nd generation (p < 0.05).Soil AN in the 4th generation was significantly higher than in the 2nd generation, but not different from that in the Pinus plantation (p < 0.05).
Soil TP was significantly lower in the Pinus plantation (0.41 g kg −1 ) than in the Eucalyptus plantations (0.90-1.07 g kg −1 ) (p < 0.05).In the Eucalyptus plantations, soil TP decreased in the 2nd generation and then recovered in the 3rd and 4th generations (Fig. 1d).Soil AP was 2.98 mg kg −1 in the Pinus plantation, but increased to 5.03 and 5.14 mg kg −1 in the 1st and 2nd generation Eucalyptus plantations, respectively, and Introduction

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Full then decreased to 2.56 and 2.93 mg kg −1 in the 3rd and 4th generations, respectively (Fig. 1g).Soil TK and AK ranged from 1.8-6.3g kg −1 and 24-92 mg kg −1 , respectively.TK was significantly lower in the Eucalyptus plantations than in the Pinus plantation, without significant differences among Eucalyptus generations (Fig. 1e).AK was significantly higher in the Pinus plantation and showed a decreasing trend with successive Eucalyptus planting (p < 0.05) (Fig. 1h).

Soil microbial biomass carbon and nitrogen
Soil MBC and MBN in our study sites ranged from 278 to 673 mg kg −1 and from 7 to 35 mg kg −1 , respectively.They were the highest in the Pinus plantation.Soil MBC decreased significantly in the 1st and 2nd generation Eucalyptus plantations and then gradually recovered in the 3rd and 4th generations.Soil MBN decreased significantly in the 2nd generation.The difference between changes in soil MBC and MBN was that MBN in the 3rd and 4th generations of Eucalyptus plantations recovered to the same level as in the Pinus plantation (Fig. 2b), but MBC in the 3rd and 4th generations of Eucalyptus plantations was significantly lower than in the Pinus plantation (Fig. 2a).The MBC/MBN ratio was significantly higher in the 2nd generation Eucalyptus plantation than in other plantations (Fig. 2c).

Soil enzyme activities
Soil BG activity was highest in the Pinus plantation and decreased with successive Eucalyptus planting (Fig. 3a).Soil CBH, PO, POD, PRO and ACP activities were the highest in the Pinus plantation.Soil CBH and POD activities decreased in the 1st and 2nd generations of Eucalyptus plantations, but gradually recovered in the 3rd and 4th generations (Fig. 3b and d).Soil PO, PRO and ACP activities decreased in the 1st generation Eucalyptus plantation, but gradually recovered in the 2nd, 3rd and 4th generations (Fig. 3c, e and g).Soil URE activity was significantly higher in the Pinus planta-Introduction

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Full tion than in the Eucalyptus plantations (p < 0.05), with no significant differences among Eucalyptus plantations (Fig. 3f).

Soil quality index
Soil pH is neither a "more is better" nor "less is better" indicator and the difference of soil pH among plantations is not significant.Except for soil pH, all soil properties were analyzed using the PCA method to identify PCs and MDS.Three PCs were selected in our study and they included eight variables (Table 1).PC1 contained SOC, TN, TK, PO, POD and ACP, which represent soil nutrient contents and enzyme activities; PC2 contained AK and PC3 contained CBH.These eight variables were used in the SQI calculation.
The SQI was calculated from the soil quality indicator scores (Table 2).The highest SQI was found in the Pinus plantation (SQI = 0.92).In the Eucalyptus plantations, the SQI significantly decreased to 0.13 in the 2nd generation plantation (p < 0.05), which was 86 % lower than in the Pinus plantation.However, in the 4th generation plantation, it had significantly recovered to 0.38 (p < 0.05), which was 59 % lower than in the Pinus plantation (Fig. 4).

Decrease in soil quality in the 1st and 2nd generation Eucalyptus plantations after converting pinus to Eucalyptus plantation
Our study found that SOC, TN, AN, TK, AK, MBC, MBN and enzyme activities significantly decreased in the 1st and 2nd generation Eucalyptus plantations after converting Pinus to Eucalyptus (Figs. 1, 2 and 3).This is consistent with many studies, which reported that SOC, TN, MBC, carbon metabolic activity and metabolic quotient were significantly lower in Eucalyptus plantations than in natural and regenerated forest or pastures (Behera and Sahani, 2003;Sicardi et al., 2004;Chen et al., 2013).However, Introduction

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Full in our study, soil TP was significantly higher in Eucalyptus plantations, which might be caused by fertilization in Eucalyptus plantations and the low mobility of phosphorus.
The decreased soil quality in the 1st and 2nd generations of Eucalyptus plantations after converting Pinus to Eucalyptus plantation may have been caused by tree species change, full reclamation, herbicide application, clear-cutting and short rotation.
Eucalyptus has a fast growth rate and a strong nutrient absorption capacity, which means that it removes and converts more nutrients from the soil into plant biomass (Laclau et al., 2005), resulting in lower nutrient contents in the soil (Fig. 1).Tesfaye et al. (2014) evaluated seven tree species for fuelwood and soil restoration and found that Eucalyptus presented the highest growth rates and biomass, but depleted soil nitrogen.The depletion of soil nitrogen in Eucalyptus plantations was also found by Wen et al. (2009).Soil nutrient levels affect soil microorganisms (Chen et al., 2013).The lower soil nutrient contents in the 2nd generation Eucalyptus plantation may lead to lower soil microbial biomass and enzyme activities and a higher MBC/MBN ratio (Figs. 2 and 3).
Full reclamation normally breaks the soil structure, exposes more aggregates and accelerates organic matter decomposition (Zinn et al., 2002), which would lead to lower soil organic matter levels in the Eucalyptus plantations.Understory vegetation may provide a better microcosm for microorganisms and alleviate storm erosion and nutrient leaching (Yu et al., 2000a), but they were destroyed in our study sites by herbicide applications during the first 3 years of Eucalyptus planting.Compared to the higher plant coverage and deeper litter layer in the Pinus plantation, the lower plant coverage and shallower litter layer in Eucalyptus plantations could not offer an appropriate protection for the broken soil structure and increased nutrient availability caused by reclamation, thus resulting in significant soil erosion and nutrient leaching.
At harvest, clear-cutting totally destroyed plant coverage and the subsequent fire clearance burned all the residues and the litter layer, which resulted in bare ground prior to Eucalyptus planting.Soil erosion and nutrient leaching can occur during heavy rainfall if there is no protection from plant and litter layers (Yu et al., 2000a).Fire also

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Full removes significant amounts of organic matter (Certini, 2005) and nutrients are lost through volatilization (Fisher and Binkley, 2000).Soil microbial biomass decreases during fire because of increased decay and death of heat-sensitive microbes or through alterations to soil physico-chemical properties (De Marco et al., 2005).These factors might be the reasons for decreased soil organic carbon, nutrient contents, microbial biomass and enzyme activities after conversion (Figs. 1, 2 and 3) in our study.
Eucalyptus cultivation rotations are very short (only 5 years) compared to Pinus (30 years), which means that there is frequent biomass loss in Eucalyptus plantations.Furthermore, short rotations have an impact on the nutrient absorption patterns and the soil nutrient returns.During the early stages of plant life, nutrient absorption is high and litter production is small, but during the later growth stages, the reverse happens (Xu, 2000).The short rotation caused Eucalyptus in the plantations at the early stages of life, which means a large nutrient absorption from the soil and a very small litter return.

Recovery in soil quality in the 3rd and 4th generation Eucalyptus plantations
Our results showed that after the sudden decline following converting Pinus to Eucalyptus, SOC, TN, MBC, CBH, PO, POD, ACP activities recovered in the 3rd and 4th generations, albeit lower than that in the native Pinus plantation (Figs. 1, 2 and 3).This is inconsistent with Yu et al. (2000b), who recorded that soil physical and chemical properties decreased during successive Eucalyptus planting.However, Lima et al. (2006) recorded an increasing soil organic matter trend as the plantation aged after Eucalyptus afforestation of degraded pastures.The inconsistency between these studies might be caused by different climate, soil properties, Eucalyptus species and management practices amongst the study sites.The soil quality recovery in the 3rd and 4th generation Eucalyptus plantations may be attributed to reduced soil disturbance and fertilizer application.Introduction

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Full Soil disturbance caused by strip reclamation in the 3rd generation Eucalyptus plantation was much smaller than full reclamation during the conversion from Pinus to Eucalyptus, which may have led to a reduction in soil organic matter decomposition, soil erosion and nutrient leaching.The decreased soil erosion, nutrient leaching and organic matter decomposition would help improving soil organic matter accumulation and nutrient levels.
Fertilization could increase plant growth and litter input (Madeira et al., 1995), which would improve soil quality.If the soil nutrient inputs through fertilization and litter fall equal the output caused by erosion, plant absorption and leaching, then soil quality would reach a steady status (Xu, 2000).Our results showed a recovery trend of soil quality in the 3rd and 4th generation Eucalyptus plantations (Fig. 4), however, we could not predict soil quality changes during more generations of Eucalyptus planting due to the lack of data.To better understand the impacts of successive Eucalyptus planting on soil quality, evaluation of more generations of Eucalyptus plantations is needed in future research.

Conclusions
Our study found that soil quality decreased significantly in the 1st and 2nd generation Eucalyptus plantations after converting Pinus to Eucalyptus plantations, but recovered in the 3rd and 4th generations, though it was still significantly lower than in the Pinus plantation.Changes in tree species, reclamation, herbicide application and long-term fertilization may contribute to the "U" shaped trend in soil quality changes during successive Eucalyptus planting.Our results emphasize the importance of long-term soil quality monitoring.Improving management practices, such as litter retention, keeping appropriate understory plant coverage and reducing soil disturbance during logging and subsequent establishment of the next plantation rotation should be considered to help improve soil quality during plantation management.Introduction

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Full  Full Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | ) Selection of representative variables.PCA was performed on the variables chosen from step (1).Only principal components (PCs) that explained at least 5 % of the variation in the data up to 85 % of the cumulative variation were examined.Within each PC, only weighted factors with absolute values within 10 % of the highest weight were retained for the MDS.(3) Redundancy reduction.Multivariate correlation coefficients were used to determine the strength of the relationships among variables.Well-correlated variables (Correlation coefficient > 0.70) were considered redundant and candidates for elimination from the data set.To choose variables within Introduction Discussion Paper | Discussion Paper | Discussion Paper | variable i .The scores of the indicators were integrated into a SQI according to Andrews et al. (2002) as follows: SQI = n i =1 Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Discussion Paper | Author contribution.H. Zheng and Z. Y. Ouyang designed the experiment and K. Zhang, F. L. Chen and Y. Wang carried them out.Y. F. Wu, J. Lan, M. Fu and X. W. Xiang helped collecting soil samples and gave suggestion about the experiment.K. Zhang and H. Zheng prepared the manuscriptDiscussion Paper | Discussion Paper | Discussion Paper | Yu, X. B., Chen, Q. B., Wang, S. M., and Mo, X. Y.: Research on land degradation in forest plantation and preventive strategies, in: Studies on Long-Term Productivity Management of Eucalyptus Plantation, edited by: Yu, X. B., China Forestry Publishing House, Beijing, 1-7, 2000a.(in Chinese) Yu, X. B., Yang, G. Q., and Li, S. K.: Study on the changes of soil properties in Eucalyptus plantation under continuous-planting practices, in: Studies on Long- Discussion Paper | Discussion Paper | Discussion Paper |

Figure 1 .Figure 2 .Figure 3 .
Figure 1.Changes in soil chemical properties during conversion of Pinus to Eucalyptus and successive Eucalyptus planting.MP, G1, G2, G3 and G4 refer to the Pinus plantation and the 1st, 2nd, 3rd and 4th generation Eucalyptus plantations, respectively.SOC, soil organic carbon; TN, total nitrogen; TP, total phosphorus; TK, total potassium; AN, alkaline hydrolytic nitrogen; AP, available phosphorus and AK, available potassium.Soil chemical properties with the same letter are not significantly different at p < 0.05.

Table 2 .
Soil quality indicator scores (mean ± standard error) for soil samples taken from the Pinus and Eucalyptus plantations.